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Botanical Sciences 99(3): 542-559. 2021 Received: November 15, 2020, Accepted: February 2, 2021 DOI: 10.17129/botsci.2795Genetic structure of threeOn line Mexican first: May bamboo 26, 2021 species Genetics / Genética A POPULATION GENETICS STUDY OF THREE NATIVE MEXICAN WOODY BamBOO SPECIES OF GUADUA (POACEAE: BamBUSOIDEAE: BamBUSEAE: GUADUINAE) USING NUCLEAR MICROSATELLITE maRKERS ESTUDIO DE GENÉTICA DE POBLACIONES DE TRES ESPECIES DE BAMBÚES LEÑOSOS NATIVOS DE MEXICO DEL GÉNERO GUADUA (POACEAE: BAMBUSOIDEAE: BAMBUSEAE: GUADUINAE) UTILIZANDO MICROSATÉLITES NUCLEARES JESSICA PÉREZ-ALQUICIRA1,2, STEPHANIE AGUILERA-LÓPEZ1, YESSICA RICO3,2, EDUARDO RUIZ-SANCHEZ*1,4 1 Universidad de Guadalajara, Laboratorio Nacional de Identificación y Caracterización Vegetal (LaniVeg), Depto. Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Zapopan, Jalisco, México. 2 CONACYT, Ciudad de México, México. 3 Red de Diversidad Biológica del Occidente Mexicano, Instituto de Ecología, A.C., Pátzcuaro, Michoacán, México. 4 Universidad de Guadalajara, Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias, Zapopan, Jalisco, Mexico. *Author for correspondence: [email protected] Abstract Background: Sporadic flowering contributes significantly to genetic diversity and connectivity among populations. Woody bamboos present sporadic or gregarious flowering patterns with long flowering cycles. In this study, we analyze the genetic diversity of three Guadua species distributed along the Gulf of Mexico slope that have different patterns of flowering. Questions: (1) Are the three Guadua species genetically differentiated? (2) Does the vulnerable species G. inermis have low levels of genetic diversity? (3) What is the relative contribution of geographic and environmental factors to the genetic structure of G. inermis? Species studied: Guadua amplexifolia, G. inermis and G. tuxtlensis. Study site and dates: During 2014 and 2015, we collected samples of G. inermis in Puebla and southeastern Mexico, G. amplexifolia in Vera- cruz and Oaxaca, and G. tuxtlensis in southern Veracruz. Methods: We successfully amplified five of nine SSR markers, and genotyped a total of 155 samples. Results: The three Guadua species were genetically differentiated. For G. inermis, we found high levels of population genetic diversity, which are relatively higher than those of other monocot species. Genetic differentiation was high and three groups were detected: north, central and south. We found a significant association between genetic distances and the maximum temperature of the warmest month, but not with geo- graphic distance. Conclusions: Our study is the first to analyze levels of genetic diversity in Mexican bamboos and confirms their taxonomic identity.G. inermis has a strong genetic structure, even when populations are geographically close. Keywords: Bamboos, genetic diversity, genetic structure, sporadic and massive flowering, polyploid. Resumen Antecedentes: La floración esporádica puede influenciar la estructura genética de las poblaciones. Los bambúes presentan patrones de floración esporádica o gregaria. En este estudio analizamos la diversidad genética de tres especies de Guadua con diferentes patrones de floración distri- buidos en la Vertiente del Golfo de México. Preguntas: 1) ¿Están las tres especies de Guadua (G. inermis, G. amplexifolia y G. tuxtlensis) genéticamente diferenciadas? 2) ¿Presenta G. inermis bajos niveles de diversidad genética? 3) ¿Cuál es la contribución relativa de los factores geográficos y ambientales en la estructura genética de G. inermis? Especies de estudio: Guadua amplexifolia, G. inermis y G. tuxtlensis. Sitio y años de estudio: En 2014 y 2015, colectamos muestras de G. inermis en Puebla y sureste de México; G. amplexifolia en Veracruz y Oaxaca, y G. tuxtlensis en el sureste de Veracruz. Métodos: Amplificamos exitosamente cinco marcadores SSR de un total de nueve y genotipificamos 155 muestras. Resultados: Las tres especies analizadas están genéticamente diferenciadas. G. inermis presentó altos niveles de diversidad genética, y superio­ res a otras especies de monocotiledóneas. Los niveles de diferenciación genética fueron altos y se detectaron tres grupos: norte, sur y centro. Encontramos una asociación significativa entre las distancias genéticas con la temperatura máxima del mes más caliente, pero no con la distancia geográfica. Conclusiones: Nuestro trabajo es el primer estudio que evalúa los niveles de diversidad genética en bambúes mexicanos y confirma su identidad taxonómica. G. inermis tiene una estructura genética alta, incluso cuando las poblaciones están cerca geográficamente. Palabras clave: Bambúes, diversidad genética, estructura genética, floración esporádica y masiva, poliploidía. This is an open access article distributed under the terms of the Creative Commons Attribution License CCBY-NC (4.0) international. https://creativecommons.org/licenses/by-nc/4.0/ 542 Pérez-Alquicira et al. / Botanical Sciences 99(3): 542-559. 2021 Understanding the processes leading to speciation and tween populations, leading to diffuse flower temporality biodiversity in plants is one of the main research topics in within a species; 4) Sporadic flowering, random or other evolutionary biology. Flowering time has a strong effect non­gregarious patterns of flowering (Troup 1921, Janzen on gene flow among populations (Fitter & Fitter 2002). 1976, Gadgil & Prasad 1984, Banik 1998, Franklin 2004, For example, floral synchrony results in the simultaneous Bhattacharya et al. 2009, Zheng et al. 2020). Understand- and massive flowering of individuals, offering abundant ing how asynchronous flowering phenology can influence floral resources that can attract numerous pollinators and patterns of gene flow in woody bamboos is crucial to elu- favoring outcrossing rates (Domínguez & Dirzo 1995, cidating its role in population genetic divergence and spe- Rodríguez­Pérez & Traveset 2016). In the same way, ciation. there is evidence that flowering synchrony increases re- The genus Guadua Kunth is one of the six genera of productive success in wind­pollinated species (Bogdzie- the subtribe Guaduinae (Judziewicz et al. 1999, Clark et wicz et al. 2020). In contrast, plant asynchrony or sporadic al. 2015, Tyrrell et al. 2018). It includes 33 species and is flowering might reduce the availability of mates and thus one of the most diverse genera in the subtribe (Clark et reproductive success in both insect and wind­pollinated al. 2015, Ruiz­Sanchez et al. 2021). Species of Guadua species (Domínguez & Dirzo 1995, Bogdziewicz et al. are distributed from Mexico to Argentina, most of the spe- 2020). Asynchrony in flowering time across populations cies occur in South America, and this region is consid- should result in lower levels of gene flow and greater ge- ered its center of diversification (Medina & Medina 1965, netic structure, even for populations that are geographi- Judziewicz et al. 1999, Londoño 2001, 2011, Clark et al. cally close together (Kirkpatrick 2000, Reisch & Posclod 2015). Mexico has seven species of Guadua: G. aculeata 2009). Rupr. ex Fourn., G. amplexifolia J. Presl., G. longifolia Geographic distance and the environment represent (E. Fourn.) R.W. Pohl, G. paniculata Munro, G. inermis key components influencing species’ genetic structure Rupr. ex Fourn, G. velutina Londoño & L.G. Clark, and G. (Rousset 1997, Wang & Bradburd 2014). Several species tuxtlensis Londoño & Ruiz­Sanchez. The last three spe- exhibit a significant pattern of isolation by distance (IBD), cies are endemic to Mexico, and except for G. paniculata, which suggests that genetic differentiation increases with which is distributed along the Pacific coast of Mexico, geographic distance. On the other hand, isolation by envi- the other species are distributed along the Gulf of Mexi- ronment (IBE) has been proposed to describe the relation- co in the states of Campeche, Chiapas, Hidalgo, Oaxaca, ship between environmental heterogeneity and the spatial Puebla, San Luis Potosí, Tabasco, Tamaulipas, and Vera- distribution of genetic variation (Wang & Bradburd 2014). cruz (Londoño & Ruiz­Sanchez 2014, Ruiz­Sanchez et Thus, genetic differentiation among populations increases al. 2020). Most of the species are used to build houses, with their environmental differentiation (Wang & Brad- fences, kiosks, and to make handicrafts (Londoño & Ruiz­ burd 2014). In contrast, limited dispersal constrains gene Sanchez 2014). flow among populations and reduces the possibility of Few studies have reported the flowering cycles ofGua - counteracting genetic drift (Slatkin 1993, Rousset 1997). dua species. Guerreiro (2014), Guerreiro et al. (2020) Woody bamboos (Poaceae: Bambusoideae: Bambuse- and Vega & Hernández (2008) recorded massive flower- ae) are a large taxonomic group with notable economic ing events and estimated flowering cycles for three South and ecological importance. Flowering in woody bamboos American Guadua species: Guadua chacoensis (Rojas) is peculiar because many of them remain in a vegeta- Londoño & P. M. Peterson (28­31 years), G. paraguayana tive phase for a long period of time, as long as decades Döll (38 years), and G. trinii (Nees) Nees ex Rupr. (30­33 or a century, followed by mass synchronous flowering years). Liebsch & Reginato (2009) estimated cycles of 27- and subsequent death (Janzen 1976). Other woody bam- 28 years between flowering events forG. sarcocarpa Lon- boos
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    CARACTERIZACIÓN GENÉTICA DE RELICTOS DE Guadua angustifolia, UN ECOSISTEMA ESTRATÉGICO DE LA ECOREGIÓN VALLE DEL CAUCA MEDIANTE STR´s TESIS DOCTORAL CARLOS ANDRES PEREZ GALINDO Sevilla, 2014 AGRADECIMIENTOS A mi madre Carmenza, abuelos, hermana, sobrino y toda mi familia que siempre ha estado allí, apoyándome en todos los procesos de materialización de mis ideas. Al profesor Heiber Cardenas, que siempre me incentivo a ir más allá en las diferentes investigaciones y en los proyectos que emprendimos, que han estado enmarcados en la construcción de nuevos programas de postgrado en Colombia, estudios en biodiversidad de nuestra gran región Vallecaucana y la puesta en marcha de diferentes proyectos para el mejoramiento formativo en ciencias biológicas de los jóvenes colombianos. A la Universidad Pablo de Olavide por el apoyo no solo académico, sino también económico en mi etapa como becario. A su excelente cuerpo profesoral, que mediante sus enseñanzas me permitieron ampliar no solo mis conocimientos en biotecnología, sino también mi visión sobre la vida, incentivándome a realizar mis estudios de postgrado en bioinformática, lo cual me permitiría tratar de entender la evolución desde la óptica molecular. Al Dr. Modesto Luceño, quien tomaría la tutoría de este importante trabajo doctoral, apoyándome en los diferentes procesos y requerimientos para la presentación de la tesis y comprendiendo las dificultades que se tienen al trabajar a distancia. A la Universidad Santiago de Cali, institución que apoyó económica, logística y moralmente la investigación objeto de este trabajo. Cuyo principal objetivo ha estado centrado en recurrir a la investigación social y científica para la defensa de la biodiversidad de cultivos nativos en una región agroindustrial, regida por los monocultivos de azúcar y que ve como la afectación de la biodiversidad incide de manera negativa en la calidad de las tierras y la disponibilidad de recursos hídricos, lo cual hoy por hoy está afectando a los habitantes de estas zonas.